Homoploid Hybrid Speciation and Recurrent Hybridization Along the Northwestern Iberian Mountain Chains

Abstract

[Abstract] Background and Aims: Natural hybridization can lead to diversification and adaptive introgression, among other outcomes. However, the mechanistic underpinnings of this process are insufficiently understood. A previous study of the Iberian endemic diploid genus Phalacrocarpum (Asteraceae, Anthemideae) identified several homoploid hybridization events and cryptic diversity, but raised questions regarding their evolutionary significance and specific genetic groups involved. This study aimed to clarify the evolutionary history of this genus. Methods: A double-digest restriction-site-associated DNA sequencing approach was used to generate nuclear single nucleotide polymorphisms (SNPs) from 261 samples of this genus and plastid sequences were obtained from 121 samples by genome skimming. Phylogenomic relationships were inferred from each of these two datasets. Bayesian genomic clustering analysis and ABBA–BABA tests were used to explore the population genetic structure and specific introgression hypotheses. Key Results: Bayesian clustering analyses identified K = 34 as the best partition for the nuclear SNP data although about half of these groups are minimally represented in each sample and are shared across taxa. The suboptimal partition K = 7 supports the existence of seven lineages. In the nuclear phylogenomic tree, P. oppositifolium subsp. anomalum and subsp. hoffmannseggii are not monophyletic. The latter and the western group of subsp. anomalum consist of several small clades, each showing varying degrees of admixture. Comparison with the plastome tree reveals cytonuclear conflict affecting mainly two taxa, suggesting historical range shifts and different hybrid origins. ABBA–BABA tests found evidence of introgression, supporting the hybrid origin of the Galician–Portuguese border group, and multiple hybridization events between P. oppositifolium subsp. anomalum and subsp. hoffmannseggii. Conclusions: Multiple, partially recurrent, hybridization events, occurring mainly along an L-shaped mountain corridor from the eastern Cantabrian range to the Serra da Estrela in central Portugal, have shaped the genetic structure of Phalacrocarpum diversity. A part of these events has resulted in three homoploid hybrid lineages, which are incipient hybrid species.